The somatotopy of speech: Phonation and articulation in the human motor cortex
Introduction
Phonation is an important “umbrella” process when thinking about human vocalization, taking account of much of the segmental aspect of speech, of suprasegmental processes like intonation (Ladd, 1996) and lexical tone (Yip, 2002), and of singing (Sundberg, 1987). Modulation of the pitch and duration of voiced sounds underlies the melodic and rhythmic aspects of speech. The older literature on intonation employed the term “melodicity” to refer to the basic acoustic stream of voicing that occurs during speech production (Fónagy, 1981, Fónagy and Magdics, 1963).
Standard models of vocal production posit the existence of a vocal “source” – i.e., subglottal air pressure from the lungs producing vibration of the vocal-folds in the airstream – followed by “filtering” of the source’s sound wave by a series of articulators in the oral and nasal cavities, to ultimately select out certain resonant frequencies in that wave. While all vowels and most consonants require phonation, some consonants can be generated in a voiceless fashion. For fricatives like the /s/ sound, this can simply involve the generation of broadband noise at the larynx in the absence of periodic vocal-fold vibration. However, the majority of the speech stream is phonated. For many languages, the proportion of a spoken sentence’s duration taken up by vowels alone is 40–50% (Ramus, Nespor, & Mehler, 1999). This does not take into account the degree of phonation that comes from voiced consonants, which would make the overall voiced component of a sentence’s duration even higher.
While phonation is a critical component of speech, neuroimaging studies have rarely recognized this point. Imaging studies of speech production reliably show activity in the ventral part of the precentral gyrus – corresponding with the somatotopic “orofacial” region of the motor and premotor cortices – and this activation has almost invariably been interpreted as reflecting articulation (e.g., Fox et al., 2001). The strong, if unspoken, assumption is that speech is first and foremost an articulatory process. Most studies that have sought to examine phonatory aspects of speech have (1) been perceptual rather than production studies (although see Barrett, Pike, & Paus, 2004), and (2) focused on suprasegmental processes like prosody or lexical tone rather than the basic speech stream. A handful of studies have tried to distinguish brain areas for articulation and phonation. For example, Murphy et al. (1997) compared vocalization of a simple phrase with silent mouthing of the phrase (to reveal phonation) and with mouth-closed vocalization of the phrase using the /a/ vowel alone (to reveal articulation). Their primary interest was in examining brain areas involved in respiration for speech. They identified a bilateral region of the sensorimotor cortex that was more active when speech breathing was involved than simple mouthing. Likewise, Terumitsu, Fujii, Suzuki, Kwee, and Nakada (2006) used independent components analysis (ICA) to contrast vocalization of a string of labial syllables with silent articulation of the string without voicing of the vowels or consonants. Their analysis revealed a bilateral region close to the classical tongue region associated with tongue movement and a left-dominant area dorsal to that involved in phonation.
Recent work from our lab has led to the characterization of a somatotopic representation of the larynx in the human motor cortex (Brown, Ngan, & Liotti, 2008). Related work from another lab has shown that this same general region contains a representation of the expiratory muscles as well (Loucks et al., 2007, Simonyan et al., 2007). In fact, this area is very close to that which Murphy et al. (1997) associated with speech breathing. (For simplicity, we will refer to this general area as the “larynx motor cortex” in this article.) Hence, the two major components that comprise the vocal source appear to be in close proximity in the motor cortex, perhaps reflecting a unique cortical-level type of respiratory/phonatory coupling specific to human vocalization; for almost all other species, this coupling occurs in the brainstem alone (Jürgens, 2002). Given that our fMRI study showed that the larynx motor cortex was activated comparably by vocal and non-vocal laryngeal tasks (i.e., vocal-fold adduction alone), this area would seem like a good candidate for being a regulator of the melodicity of complex human vocalizations such as speaking and singing.
In order to examine the phonatory component of speech, we analyzed motor cortex activations for a speech production task in comparison to elemental control tasks for tongue movement, lip movement, and monotone vowel phonation, with the intent of looking for potential additivity. In a second study, we used activation likelihood estimation (ALE) meta-analysis to compare a previously-published meta-analysis of word production (Turkeltaub, Eden, Jones, & Zeffiro, 2002) with a new meta-analysis of simple phonation, namely syllable production. The goal of the combined analysis was to characterize the neural contribution of phonation to speech production, a point that has been absent in most previous neuroimaging analyses of speech production.
Section snippets
Subjects
Sixteen subjects (eight males, eight females), with a mean age of 28.4 years (ranging from 21 to 49 years), participated in the study after giving their informed consent (Clinical Research Ethics Board, University of British Columbia). Each individual was without neurological, psychiatric or audiological illness. Subjects were all fluent English speakers but were unselected with regard to handedness. Three of the subjects were left-handed.
Tasks
Subjects performed six oral tasks (one task per fMRI
fMRI
An analysis of the speech task vs. rest (Fig. 1 and Table 1) showed bilateral activations in the part of the motor/premotor cortex that Brown et al. (2008) identified as the larynx representation, showing ventromedial peaks (slice at z of 32) and dorsolateral peaks (slice at z of 40). A second major activation focus in the motor cortex was found in the Rolandic operculum, which we showed previously contains, at least in part, the ventral portion of the somatotopic tongue representation (Brown
Discussion
In this study, we attempted to look at speech in a somatotopic manner, and especially to illuminate the role of phonation in speech production. We use these analyses to formulate a general model of vocalization in the brain.
Conclusions
Using two complementary comparisons between speech and non-speech oral tasks (fMRI and meta-analysis), we have attempted to disentangle phonation and articulation in speech, and have shown that motor-control models like the “source-filter” model can be represented somatotopically in the motor cortex. A principal site of activation for speech is the larynx representation in the motor cortex, in keeping with the overwhelmingly voiced nature of speech. Additional activity in the Rolandic operculum
Acknowledgments
This work was supported by a grant to SB from the Grammy Foundation. ARL and SMT were supported by the Human Brain Project of the NIMH (R01-MH074457-01A1), and PQP by NSF grant 0642592. We thank Trudy Harris, Jennifer McCord, and Burkhard Mädler at the MRI Research Centre of the University of British Columbia for expert technical assistance. We thank Roger Ingham (University of California at Santa Barbara) for critical reading of a previous version of the manuscript.
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